The piece of intensively-produced supermarket meat you eat today could easily kill you and your children in years to come. Vancomycin Resitant enterococci,Salmonella Typhimurium DT104,Campylobacter Coli, could all lie dormant in your gut, waiting for your immune system to go down. Go veggie or at least organic

If Max eats up all his chicken, he'll grow to be a big, strong boy. Unless it kills him first

Bacteria from the cut-price meat that we eat can remain in the gut for years and, warn scientists, breed superbugs untreatable in humans. So are we sitting on an antibiotic-resistant time bomb?

Andrew Purvis Sunday August 10, 2003 The Observer

Even as you pick up the tray of cut-price chicken thighs, your life expectancy has plummeted. Ten years from now, as a result of this penny-pinching impulse buy, you could die - untreatable by modern medicine - in the intensive-care unit of a British hospital, the victim of a killer bug implanted in your gut and waiting for its Big Moment. It's a complex tale of poor slaughterhouse hygiene, gene transfer, microbiology and pure chance, but at its centre is the antibiotic avoparcin - a 'growth promoter' once given to chickens and pigs to help them gain weight efficiently. Though our story is about poultry, it could just as easily be about the pork chop, sausages, or salami sticks in your shopping basket. When you read this, you will understand why the check-out staff at supermarkets put your meat in a bag separate from your tomatoes; you will realise the importance of food hygiene and appreciate the true danger of cross-contamination.

Banned in Europe since 1997 due to fears about human health, avoparcin is no longer used or manufactured anywhere in the world - yet its legacy remains in the environment, and in the guts of animals generations later. Because it was given at very low dosages (fewer than 50 parts per million in feed or drinking water), avoparcin didn't kill bacteria outright but allowed some - the most resistant to it - to survive. Exposed to other drugs, these can in turn become more resistant to several antibiotics, creating a 'superbug'.

At the time of purchase, it has to be said, the chicken's pathology is relatively benign - if a little unsavoury. Most farm animals, and indeed most humans, carry millions of harmless bacteria called enterococci in their faeces and gut - and these can be transferred to the surface of meat at slaughter, often through unclean blades or the mechanical scoops inserted through the birds' backsides to eviscerate them. As the chicken oozes unappetisingly on the top shelf of your fridge, wrapped in a leaky carrier bag, blood drips on to the cheddar cheese below - the classic 'cross contamination' sequence - and seeps through its paper wrapper.

Making yourself a cheese sandwich next day, you don't notice the bacteriological accompaniment - but you have inadvertently eaten uncooked enterococci. As the chicken itself is grilled for dinner, atomising the evidence and rendering the meat safe, the microbiological time bomb is ticking away in your stomach. Because the enterococci are harmless, you notice no symptoms. For a few days, the bugs struggle to survive inside their new human host - and they will quickly die. But before they do, they will pass on their gene for antibiotic resistance (acquired through repeated exposure to avoparcin) to other bacteria, notably enterococcus faecalis and enterococcus faecium, bugs that live in the gut of humans.

'We now know there are little pieces of mobile DNA,' says Professor Laura Piddock, Professor of Microbiology at Birmingham Medical School, 'which can detach themselves from the animal enterococcus and jump across to the human type. It's a form of bacterial sex. You then have a resistant bacterium in your body, which can sit there waiting in your gut. You don't know when you ate the resistance gene - it could have been last week, it could have been 10 years ago. It isn't a problem if you're a normal, healthy individual, but if you go into hospital for a kidney transplant or similar operation, you will be very vulnerable. You can be infected by that organism or, worse, it can spread through an entire hospital ward through the oral-faecal route.'

In other words, if you don't wash your hands, resistant bacteria can attach themselves to food, cutlery, bed linen, clothing and surgical instruments, infecting wards and colonising the intestines of other patients. In the physically robust, these human enterococci can cause minor urinary infections and stop wounds healing. In the less strong - such as long-term hospital patients, people with kidney failure, the elderly and anyone with a compromised immune system - they can lead to raging infections of the blood stream (bacteraemia), heart muscle (endocarditis) and brain (meningitis), often resulting in death. And so, when you are admitted to hospital for minor heart surgery a decade after you ate that tainted cheddar sandwich, the superbugs are waiting to colonise your chest and kill you.

Known as VRE (Vancomycin Resistant Enterococci), these bugs are among the most indestructible isolated from humans and are virtually untreatable in their most resistant form. Though minor infections usually respond to penicillins, macrolides or tetracyclines - three families of antibiotics in widespread use today - there is nothing modern medicine can do about the more serious outbreaks. In the past, doctors used two expensive and potentially toxic medicines, teicoplanin and vancomycin, injected by syringe. In 1986, however, the first vancomycin-resistant enterococcus was found in France and, a year later, it was isolated in the UK. Similar bacteria with 'multiple resistance' have been found worldwide, including the US - and there is nothing left in the medical armoury to treat them. 'These are infections of the 1990s, 2000 and beyond,' says Professor Piddock. 'Due to advances in modern medicine, which have ensured that seriously ill patients tend to live, we are seeing a whole new spectrum of diseases, some of which are very difficult to treat- including VRE.'

One of the main reasons is the widespread use of antibiotic growth promoters such as avoparcin - which is chemically related to vancomycin (both are classed as glycopeptides). 'As long ago as 1969,' Professor Piddock explains, 'the Swann Committee [commissioned by the Government] recommended that no agent used in human medicine should be used for growth promotion in animals - and people have stuck to that. However, there are drugs used in animals with a different name and chemical structure which are so similar to those used in people that the bacteria cannot distinguish between the two. As far as they are concerned, it is the same molecule - so they become resistant to the human drug.'

One such drug is ciprofloxacin, the antibiotic many Americans turned to when anthrax attacks were threatened after 11 September 2001. It is one of the fluoroquinolones, a family of antibiotics that includes several used to treat farm animals, mainly chickens and turkeys. 'We're particularly concerned about this one,' says Dr Caroline Willis, a clinical scientist with the Health Protection Agency in Southampton, 'because it is a first-line agent for treating serious hospital infections.' It is also the first line in drugs for fighting salmonella, E. coli and campylobacter - serious food-poisoning bugs that affect 100,000 people in England and Wales each year and account for 100 to 200 deaths. Campylobacter poisoning, though its symptoms are the least severe, is on the increase, with cases doubling since 1990. Last year, 60,000 people fell victim to it and 80 died. Of those 60,000, an estimated 9,000 would have had the ciprofloxacin-resistant strain which may not respond to that particular medicine. It is Dr Willis's job to look for bacteria in food and find out how resistant they are to human medicines. In a recent examination of raw chicken imported from Thailand and Brazil, she found that 78 per cent of the campylobacter bacteria isolated were resistant to ciprofloxacin (compared to 10 per cent in UK samples); among E. coli bacteria, 47 per cent were resistant (compared to zero resistance in chicken produced in Britain). 'This suggests that a drug related to ciprofloxacin is being used quite freely in chicken production in these countries,' Dr Willis concludes. 'Because 20 to 30 per cent of our chicken is imported from places like Thailand, we are sitting on an antibiotic-resistant time bomb.'

What Dr Willis means is a situation where more and more bacteria fail to respond to treatment - allowing human diseases to run rampant, as in the pre-antibiotic era. Already, the food-poisoning bug Salmonella typhimurium DT104 is resistant to ampicillin, chloramphenicol, streptomycin, sulfonamides and tetracycline (all used in human medicine) and is failing to respond to trimethoprim and ciprofloxacin as well. Between 1990 and 1996, there was a tenfold increase in DT104 cases in Britain - though this has been brought under control by mass vaccination of poultry - and this strain results in twice as many hospitalisations and 10 times as many fatalities as other types of foodborne salmonella. In 1998, the most serious recorded outbreak occurred in Denmark, when 22 people fell ill after eating infected pork. Of those, seven were admitted to hospital and four failed to respond to treatment with fluoroquinolone (the antibiotic of choice for serious food-poisoning episodes). One previously healthy 62-year-old woman died due to intestinal perforation, after a five-day course of fluoroquinolone failed to kill the resistant bacteria before surgery.

Nor is it just DT104 that is failing to respond to first-line drug regimes. 'In campylobacter coli, a strain of the food-poisoning bug which originated in pigs, human resistance to erythromycin is now running at 13 per cent,' says Richard Young, policy adviser to the Soil Association. 'It's the only safe drug used to treat children with the infection, so we are talking about 200 to 300 children per year who will be untreatable with this drug.' Erythromycin is one the macrolides family, banned as growth promoters in 1999. 'Since then,' says Young, 'the quantity prescribed by vets has actually gone up, from 23 tonnes in 1998 to 55 tonnes now - which is a move in the wrong direction. I believe that, literally within a decade or so, we are going to see a large number of people dying from drug-resistant infections for which there are simply no effective antibiotics.'

The culprit, he believes, is the indiscriminate use of antibiotics in food animals - and in this he is not alone. After hearing evidence from the World Health Organisation and others in 1997, the EU banned avoparcin because of fears about resistant superbugs spreading from poultry to humans. In 1999, both Tesco and Marks & Spencer said they would no longer stock chickens that had been fed antibiotic growth promoters (AGPs), and EU legislation in the same year outlawed six more. This leaves only four such products (avilamycin, flavomycin, monensin and salinomycin) licensed for farm use - and these, too, will be withdrawn from all EU countries, including Britain, by January 2006.

In June this year came further evidence that the tide against antibiotic growth promoters was turning. In a well-publicised announcement, the McDonald's fast food company in Illinois directed some of its meat suppliers to stop using AGPs by the end of 2004 while telling others to cut back. The total ban applies mainly to suppliers of chicken, who routinely use 24 growth promoters which are closely related to human medicines - including virginiamycin, believed to be the cause of outbreaks of the VRE super-bug in the US. 'We would love to be a catalyst for change industry-wide on antibiotic use,' said Robert Langert, McDonald's senior director for social responsibility. 'People have been arguing about this all night and day, but now we are taking some practical steps and expect we'll make some real progress.'

It isn't the first time such a clarion call for reform has been issued by a major player in the food world - and last time the tune was short-lived. In 2000, British poultry farmers working under the Assured Chicken Production scheme - represented by the Little Red Tractor logo, and accounting for 85 per cent of all chickens sold in the UK - agreed very publicly to discontinue the use of antibiotic growth promoters. In 2002, however, a clause was added to the ACP standard, saying AGPs could be used preventatively in feed 'under veterinary supervision on welfare grounds' - and this remains the case, though the guidelines are currently under review. 'They claim the drugs are necessary to control disease,' says Richard Young of the Soil Association, 'but using them in this way is not permitted in the EU.' Antibiotic growth promoters, which are classed as feed additives, have never been evaluated for safety as veterinary medicines. In May this year, Margaret Beckett, the Secretary of State for Agriculture, agreed. In a letter to the Soil Association - the licensing body for organic farming, which is lobbying for a radical reform of intensive farming methods - she admitted that using growth promoters in this way 'could be illegal under EU legislation' and resolved to look into the matter. For its part, Assured Chicken Production says preventative use of AGPs reduces the need for therapeutic antibiotics - the ones, they say, which are more closely related to human medicines.

In fact, growth promoters are only the tip of the antibiotic iceberg. While 43 tonnes of AGPs (measured by weight of active ingredients) were sold in Britain in 2001, the overall quantity of antibiotics used on farm animals was 463 tonnes - more than 10 times as much. This figure has risen from 452 tonnes since 1998, sug gesting that the fears voiced by medical experts have largely gone unheeded. Though the up-to-date total will be less (due to the phasing out of AGPs and some drugs used in human medicine), a 1998 report for MAFF - now Defra, the Department for Environment, Food and Rural Affairs - listed no fewer than 61 antimicrobials used to treat farm animals which had implications for human health. These were those antibiotics used in agriculture 'which may affect the antimicrobial resistance status of foodborne pathogens, or contribute to the resistance pool in man'.

In addition to these, Richard Young is worried by the coccidiostats, powerful drugs such as nicarbazin, lasalocid and narasin which are used to treat parasitic infections in poultry and game. While the Veterinary Medicines Directorate (VMD), which monitors residues in food animals, says 99 per cent of poultry and 97 per cent of eggs are free of such chemicals, Young believes the figures could be wrong by as much as 2,000 per cent due to the way in which data is collected. He claims that four per cent of all eggs and 10 per cent of all chicken livers tested in the UK contain residues of coc cidiostats, some of which are toxic in high dosages and cause irregular heart activity.

Pigs, too, are routinely fed or injected with up to 10 antibiotics in their lifetime (on average, 15g of medicine for every pig reared in Britain, compared to 4g per pig in Denmark), while lambs may be given 'antihelmintics' to control outbreaks of nematodirus disease (caused by a parasitic worm) and most dairy cattle will have antibiotics pumped directly into their teats to fend off mastitis. However, because all food animals in Britain are subject to a 'withdrawal period' before slaughter, allowing antibiotics to be purged from the system, it is unlikely that such drugs enter the food chain in sufficient quantities to affect our health. However, as Richard Young points out, not all farmers abide by the rules governing withdrawal - and poultry farmers in particular sell off smaller, surplus birds ahead of the main flock (known as 'thinning') before they are taken off drugs. Could the occasional antibiotic residue, which scientists say can't exist, cause an allergic reaction and make some people ill?

Steven Saunders, chef-proprietor of the Sheene Mill Hotel and Restaurant in Melbourn, Cambridgeshire, is convinced they can. 'My mother never gave me penicillin because I reacted badly to it,' he says, 'and to me it makes perfect sense that I'm allergic to antibiotics in meat. I can enjoy a meal, I can have dinner with friends - but if I eat the chicken, I know how I will feel next day. My stomach churns, I'm out of sorts. It's the same with Indian food: I can cook it myself and never suffer - but if I go to an Indian restaurant, I probably have the cheapest form of catering chicken that is intensively farmed, and I know it's going to get me. By the next morning, it has.'

Long before organic food was fashionable - or even a household term - Saunders began eating a chemical-free diet and serving naturally-reared meat in his restaurant. 'I sourced my ducks from Aylesbury,' he says, 'my chickens from a place near Thetford - and my restaurant at the time, called the Pink Geranium, started getting incredible reviews.' By using meat that was free of antibiotics, Saunders became better known as a chef and found himself ideally positioned to be an outspoken advocate of organic farming - but is meat produced in this way really any safer? 'From a microbiological point of view,' says Professor Piddock, 'I doubt it. Organically reared animals carry the same bugs, they get ill, they are treated with antibiotics - but probably less than in conventional farming. They have a better life, they are healthier, and organic meat certainly tastes better. That, I imagine, is more to do with diet than a lower dependency on antibiotics.'

Despite Saunder's organic zeal, the science also suggests that stopping the routine use of antibiotics in food production may not be the answer. When Denmark banned avoparcin (in 1995) and virginiamycin (in 1998), there was initially an encouraging result. The proportion of avoparcin-resistant enterococci found in chickens fell from 73 per cent to five per cent in a five-year period, while the fraction of virginiamycin-resistant enterococci almost halved. But the decrease in resistance came at a price in terms of animal welfare, with higher mortality rates in young pigs (which are also fed avoparcin) and an increased incidence of gastroenteritis. In both Denmark and Sweden, the amount of antibiotics prescribed therapeutically by vets has risen since growth promoters were banned, reflecting a higher incidence of sickness in animals.

'That may be true,' says Steven Saunders, 'but that is because the whole farming system needs a rethink. The only reason animals are given these antibiotics is because they are living in such terrible conditions. They are produced intensively simply to keep up with demand - but why do we need all this cheap meat - the sausages, the burgers, the chicken tikka masala? I think we eat too much meat anyway, so farmers don't have to produce all these thousands of chickens, do they? People can eat pasta instead, until meat is a quality product again.'

For the time being, that quality product does come from animals reared organically. Living under better welfare conditions, they don't need antibiotics administered constantly in their feed or given prophylactically (as an insurance policy against disease, rather than as a treatment). However, they may be given the odd homeopathic remedy. 'Most organic farms will use homeopathy to some extent,' says Will Best, who keeps 140 dairy cows, 100 younger cattle and 100 ewes on his 500-acre farm near Cerne Abbas in Dorset. 'We have a herdsman, Phil Hansford, who has developed an in-depth understanding of it. He wrote The Herdsman's Introduction to Homeopathy which nearly all the organic herdsmen have . '

Under Hansford's guidance, a cow suffering from pneumonia was once prescribed beryllium instead of the vet's antibiotics, followed by two further remedies for ticks (which were challenging her immune system) and swollen lymph glands. 'That required considerable input, intelligence and detective work,' says Best, 'but after a few days the cow got better. I cannot remember the last time we used an antibiotic on a bovine, though we have done occasionally on sheep. As far as the cattle are concerned, the situation just doesn't arise - and I think this shows in the quality and purity of our milk, which is sold under the Manor Farm label.'

In conventional dairy farming, Best explains, the main antibiotic use is what is known as dry-cow therapy. 'The average cow does about 10 months milking, followed by two months off before she calves again,' says Best, 'and in that period, a dose of long-acting antibiotic is pushed up each of the cow's teats to prevent mastitis. The idea is that, during the dry period, the antibiotic won't be flushed out by the milk.' However, such are fears about antibiotic resistance, a product has been developed by Pfizer in New Zealand which eliminates the need for drugs. Teatseal is a chemically inert silicone plug pushed up the cow's teat canal to seal it, preventing bacteria from entering. 'It's marvellous for the trade,' says Best, 'because they sell it at the same price as the antibiotic.' However, the product is good news for the consumer as well. 'If the average dairy farmer follows this recommendation,' Best calculates, 'the routine use of antibiotics in milk will come down by 50 to 60 per cent.'

For the time being, antibiotic use on farms in Britain continues to rise - and even if this were reversed, its legacy would continue. According to the World Health Organisation, there is now a variant of Salmonella typhimurium DT104 (resistant to at least seven human antibiotics) which has multiple resistance built into its genetic make-up permanently. In other words, even if antimicrobial drugs were banned completely in food animals, the variant known as R-type ACSSuT would remain resistant to these human medicines.

More disconcertingly, research conducted in 2001 suggests that one in 10 British children under the age of 10 may carry multi-resistant superbugs in their digestive systems, limiting the drug options available to them. Researchers at St Bartholomew's Hospital found that 11 per cent of stool samples contained bacteria such as E. coli that were resistant to chloramphenicol, a drug rarely given to children - suggesting they had acquired resistance without having taken the antibiotics. Though animal antimicrobials were not directly implicated, a spokesman for the Public Health Laboratory Service said: 'The usage of antibiotics is the driving factor in the development of resistance. Therefore, ways of reducing resistance must focus on the amount of antibiotics to which the population is exposed.' Though the drugs prescribed at doctors' surgeries certainly play a part, half the antibiotics dispensed in Britain every year are used in our food.

What it is: A bacterium in the faeces and gut of humans, dangerous if spread through poor hygiene. Common in hospital wards. A different type of drug-resistant enterococcus is carried by chickens and pigs, and this transfers its 'resistance gene' to the human bacterium, making it untreatable.

Resistant to: Vancomycin, the most powerful human antibiotic available. Also teicoplanin, the penicillins, the macrolides and the tetracyclines.

Cases: No official figures, but one study found VRE present in the stools of 15 per cent of kidney patients and 2 per cent of the general population (1.2m people). But VRE can now pass on its resistance gene to MRSA (Methicillin Resistant Staphylococcus Aureus), a hospital 'superbug' infecting at least 13,000 patients a year for whom vancomycin is the last defence.

What it is: A resistant strain of campylobacter, the fastest growing food-poisoning bug.

Resistant to: Erythromycin, the only safe antibiotic for treating food-poisoning in children. Campylobacter strains in general are resistant to ciprofloxacin.

Cases: Campylobacter accounted for 60,000 poisonings and 80 deaths last year. In 9,000 cases, the bug was resistant to ciprofloxacin. Each year, 200-300 children with it are untreatable with erythromycin.

Symptoms: Gastroenteritis with fever, abdominal cramps and diarrhoea that is often bloody. It can be fatal.

Likely culprit: The macrolides - antibiotic growth promoters (now banned) - given mainly to pigs and still prescribed therapeutically by vets in UK. In ciprofloxacin resistance, enrofloxacin - still licensed for use in poultry - implicated.